{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,19]],"date-time":"2026-09-19T19:06:38Z","timestamp":1789844798845,"version":"4.0.1"},"reference-count":67,"publisher":"Wiley","issue":"4","license":[{"start":{"date-parts":[[2026,1,14]],"date-time":"2026-01-14T00:00:00Z","timestamp":1768348800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"},{"start":{"date-parts":[[2026,1,14]],"date-time":"2026-01-14T00:00:00Z","timestamp":1768348800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32471768"],"award-info":[{"award-number":["32471768"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Plant Cell &amp; Environment"],"published-print":{"date-parts":[[2026,4]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>\n                    Increasing evidences show plant growth\u2010promoting rhizobacteria (PGPR) benefit legume\u2010rhizobium symbiosis, and iron\u2010based nanoparticles (FeNPs) act as rhizobia microenvironment stabilizers. However, few studies explored if their combination exerts synergistic effects on the symbiosis in legume. Here, we compared the effects of FeNPs,\n                    <jats:italic>Pseudomonas rhizovicinus<\/jats:italic>\n                    M30\u201035, and their co\u2010application (Fe\u2009+\u2009M) on alfalfa growth, nitrogen fixation, root metabolites, and rhizosphere microbiome. Compared with FeNPs and M30\u201035, Fe\u2009+\u2009M increased shoot height, root length, root activity, chlorophyll content, and net photosynthetic rate (Pn) by 63.2% and 45.4%, 61.1% and 70.6%, 56.2% and 47.1%, 20.1% and 18.6%, and 41.1% and 30.6%, respectively; the nodule number, nitrogenase activity, ureide content, and leghemoglobin content rose by 29.6% and 31.4%, 58.5% and 78.7%, 20.4% and 15.1%, and 9.7% and 12.4%, respectively. Metabolomic analysis showed that Fe\u2009+\u2009M enhanced the accumulation of benzenoid compounds in roots, while microbial co\u2010occurrence network analysis indicated reduced complexity and connectivity of rhizosphere bacterial and fungal communities. Importantly, core microbes, such as\n                    <jats:italic>Hydrogenophaga<\/jats:italic>\n                    ,\n                    <jats:italic>Nocardioides<\/jats:italic>\n                    ,\n                    <jats:italic>unidentified_Mitochondria<\/jats:italic>\n                    , and\n                    <jats:italic>Scedosporium<\/jats:italic>\n                    , were positively associated with benzenoid compounds, which contribute to nutrient cycling in the rhizosphere. Our findings demonstrate that FeNPs and PGPR strain together achieve synergistic effects on the nitrogen fixation in alfalfa.\n                  <\/jats:p>","DOI":"10.1111\/pce.70387","type":"journal-article","created":{"date-parts":[[2026,1,15]],"date-time":"2026-01-15T04:07:49Z","timestamp":1768450069000},"page":"2278-2291","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Synergy of FeNPs and PGPR Strain Enhances Nitrogen Fixation by Linking Root Metabolites and Rhizosphere Microbiome Assembly in Alfalfa"],"prefix":"10.1111","volume":"49","author":[{"given":"Mingxu","family":"Zhang","sequence":"first","affiliation":[{"name":"State Key Laboratory of Herbage Improvement and Grassland Agro\u2010ecosystems; Center for Grassland Microbiome; College of Pastoral Agriculture Science and Technology Lanzhou University Lanzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ruiquan","family":"Ding","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Herbage Improvement and Grassland Agro\u2010ecosystems; Center for Grassland Microbiome; College of Pastoral Agriculture Science and Technology Lanzhou University Lanzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tingyuan","family":"Jia","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Herbage Improvement and Grassland Agro\u2010ecosystems; Center for Grassland Microbiome; College of Pastoral Agriculture Science and Technology Lanzhou University Lanzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhiguo","family":"Wu","sequence":"additional","affiliation":[{"name":"School of Physical Science and Technology Lanzhou University Lanzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Muzammil","family":"Hussain","sequence":"additional","affiliation":[{"name":"College of Agriculture and Food Engineering Baise University Baise China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li","family":"Wang","sequence":"additional","affiliation":[{"name":"College of Life and Environmental Sciences, State &amp; Local Joint Engineering Research Center for Ecological Treatment Technology of Urban Water Pollution, Zhejiang Provincial Key Lab for Water Environment and Marine Biological Resources Protection, Zhejiang Provincial Collaborative Innovation Center for Tideland Reclamation and Ecological Protection Wenzhou University Wenzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gary Y.","family":"Gan","sequence":"additional","affiliation":[{"name":"College of Life and Environmental Sciences, State &amp; Local Joint Engineering Research Center for Ecological Treatment Technology of Urban Water Pollution, Zhejiang Provincial Key Lab for Water Environment and Marine Biological Resources Protection, Zhejiang Provincial Collaborative Innovation Center for Tideland Reclamation and Ecological Protection Wenzhou University Wenzhou China"},{"name":"Agroecosystems, The uBC\u2010Soil Group Tallus Heights Kelowna British Columbia Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3562-920X","authenticated-orcid":false,"given":"Jinlin","family":"Zhang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Herbage Improvement and Grassland Agro\u2010ecosystems; Center for Grassland Microbiome; College of Pastoral Agriculture Science and Technology Lanzhou University Lanzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,1,14]]},"reference":[{"key":"e_1_2_8_2_1","doi-asserted-by":"publisher","DOI":"10.1007\/s42729-020-00302-1"},{"key":"e_1_2_8_3_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00374-012-0705-2"},{"key":"e_1_2_8_4_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jenvman.2023.118572"},{"key":"e_1_2_8_5_1","doi-asserted-by":"publisher","DOI":"10.1111\/jam.14754"},{"key":"e_1_2_8_6_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2303439121"},{"key":"e_1_2_8_7_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2013.00359"},{"key":"e_1_2_8_8_1","doi-asserted-by":"publisher","DOI":"10.1021\/acsnano.1c08977"},{"key":"e_1_2_8_9_1","doi-asserted-by":"publisher","DOI":"10.1038\/nmeth.f.303"},{"key":"e_1_2_8_10_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41396-023-01521-x"},{"key":"e_1_2_8_11_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0027317"},{"key":"e_1_2_8_12_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00374-024-01886-x"},{"key":"e_1_2_8_13_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00284-020-01971-y"},{"key":"e_1_2_8_14_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11427-024-2876-0"},{"key":"e_1_2_8_15_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.indcrop.2023.116698"},{"key":"e_1_2_8_16_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.adk1412"},{"key":"e_1_2_8_17_1","doi-asserted-by":"publisher","DOI":"10.1038\/nrmicro1129"},{"key":"e_1_2_8_18_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.plaphy.2021.02.003"},{"key":"e_1_2_8_19_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10482-021-01612-9"},{"key":"e_1_2_8_20_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41588-025-02164-8"},{"key":"e_1_2_8_21_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00425-002-0920-4"},{"key":"e_1_2_8_22_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tplants.2025.02.002"},{"key":"e_1_2_8_23_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2318692121"},{"key":"e_1_2_8_24_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41565-019-0439-5"},{"key":"e_1_2_8_25_1","doi-asserted-by":"publisher","DOI":"10.1021\/acs.est.3c07850"},{"key":"e_1_2_8_26_1","doi-asserted-by":"publisher","DOI":"10.1021\/acsnano.4c15823"},{"key":"e_1_2_8_27_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41565-023-01392-5"},{"key":"e_1_2_8_28_1","doi-asserted-by":"publisher","DOI":"10.1021\/acsnano.3c02783"},{"key":"e_1_2_8_29_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jhazmat.2022.129294"},{"key":"e_1_2_8_30_1","doi-asserted-by":"publisher","DOI":"10.1093\/ismejo\/wrae210"},{"key":"e_1_2_8_31_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41565-024-01667-5"},{"key":"e_1_2_8_32_1","doi-asserted-by":"publisher","DOI":"10.1093\/hr\/uhae220"},{"key":"e_1_2_8_33_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.xplc.2025.101372"},{"key":"e_1_2_8_34_1","doi-asserted-by":"publisher","DOI":"10.1186\/s12951-022-01372-2"},{"key":"e_1_2_8_35_1","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btr507"},{"key":"e_1_2_8_36_1","doi-asserted-by":"publisher","DOI":"10.1111\/plb.13417"},{"key":"e_1_2_8_37_1","doi-asserted-by":"publisher","DOI":"10.1186\/s13213-025-01793-y"},{"key":"e_1_2_8_38_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.micres.2025.128084"},{"key":"e_1_2_8_39_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.scitotenv.2023.167871"},{"key":"e_1_2_8_40_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-phyto-010824-023359"},{"key":"e_1_2_8_41_1","doi-asserted-by":"publisher","DOI":"10.1093\/ismejo\/wrae223"},{"key":"e_1_2_8_42_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF00028813"},{"key":"e_1_2_8_43_1","doi-asserted-by":"publisher","DOI":"10.3390\/microorganisms9081561"},{"key":"e_1_2_8_44_1","first-page":"3213","article-title":"Effect of a Zinc Phosphate Shell on the Uptake and Translocation of Foliarly Applied ZnO Nanoparticles in Pepper Plants (Capsicum annuum)","volume":"58","author":"Rodrigues S.","year":"2024","journal-title":"Environmental Science & Technology"},{"key":"e_1_2_8_45_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2016.00815"},{"key":"e_1_2_8_46_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1462-2920.2007.01564.x"},{"key":"e_1_2_8_47_1","doi-asserted-by":"publisher","DOI":"10.1126\/sciadv.abh2433"},{"key":"e_1_2_8_48_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2024.10.015"},{"key":"e_1_2_8_49_1","doi-asserted-by":"publisher","DOI":"10.1021\/acs.est.0c03767"},{"key":"e_1_2_8_50_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41579-020-0412-1"},{"key":"e_1_2_8_51_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-025-09057-0"},{"key":"e_1_2_8_52_1","doi-asserted-by":"publisher","DOI":"10.1021\/acs.est.3c10506"},{"key":"e_1_2_8_53_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.soilbio.2025.109738"},{"key":"e_1_2_8_54_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-025-56226-w"},{"key":"e_1_2_8_55_1","doi-asserted-by":"publisher","DOI":"10.1021\/acssuschemeng.3c00954"},{"key":"e_1_2_8_56_1","doi-asserted-by":"publisher","DOI":"10.1111\/nph.19697"},{"key":"e_1_2_8_57_1","doi-asserted-by":"publisher","DOI":"10.1186\/s12951-024-02537-x"},{"key":"e_1_2_8_58_1","doi-asserted-by":"publisher","DOI":"10.1111\/pce.14478"},{"key":"e_1_2_8_59_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-017-18055-w"},{"key":"e_1_2_8_60_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.scitotenv.2019.134433"},{"key":"e_1_2_8_61_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.micres.2025.128078"},{"key":"e_1_2_8_62_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jplph.2022.153708"},{"key":"e_1_2_8_63_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.biortech.2023.129987"},{"key":"e_1_2_8_64_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.xplc.2024.101045"},{"key":"e_1_2_8_65_1","first-page":"12","article-title":"Advances in Basic Biology of Alfalfa (Medicago sativa L.): a Comprehensive Overview","volume":"7","author":"Zhang Y.","year":"2025","journal-title":"Horticulture Research"},{"key":"e_1_2_8_66_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.soilbio.2023.109100"},{"key":"e_1_2_8_67_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.molp.2023.03.009"},{"key":"e_1_2_8_68_1","doi-asserted-by":"publisher","DOI":"10.1093\/jxb\/erl259"}],"container-title":["Plant, Cell &amp; Environment"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/pce.70387","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1111\/pce.70387","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/pce.70387","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,6,22]],"date-time":"2026-06-22T11:45:49Z","timestamp":1782128749000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/pce.70387"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,1,14]]},"references-count":67,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2026,4]]}},"alternative-id":["10.1111\/pce.70387"],"URL":"https:\/\/doi.org\/10.1111\/pce.70387","archive":["Portico"],"relation":{},"ISSN":["0140-7791","1365-3040"],"issn-type":[{"value":"0140-7791","type":"print"},{"value":"1365-3040","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,1,14]]},"assertion":[{"value":"2025-08-10","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-01-05","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-01-14","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}